Responses of Aspen Leaves to Heatflecks: Both Damaging and Non-Damaging Rapid Temperature Excursions Reduce Photosynthesis

During exposure to direct sunlight, leaf temperature increases rapidly and can reach values well above air temperature in temperate forest understories, especially when transpiration is limited due to drought stress, but the physiological effects of such high-temperature events are imperfectly understood. To gain insight into leaf temperature changes in the field and the effects of temperature variation on plant photosynthetic processes, we studied leaf temperature dynamics under field conditions in European aspen (Populus tremula L.) and under nursery conditions in hybrid aspen (P. tremula × P. tremuloides Michaux), and further investigated the heat response of photosynthetic activity in hybrid aspen leaves under laboratory conditions. To simulate the complex fluctuating temperature environment in the field, intact, attached leaves were subjected to short temperature increases (“heat pulses”) of varying duration over the temperature range of 30 °C–53 °C either under constant light intensity or by simultaneously raising the light intensity from 600 μmol m−2 s−1 to 1000 μmol m−2 s−1 during the heat pulse. On a warm summer day, leaf temperatures of up to 44 °C were measured in aspen leaves growing in the hemiboreal climate of Estonia. Laboratory experiments demonstrated that a moderate heat pulse of 2 min and up to 44 °C resulted in a reversible decrease of photosynthesis. The decrease in photosynthesis resulted from a combination of suppression of photosynthesis directly caused by the heat pulse and a further decrease, for a time period of 10–40 min after the heat pulse, caused by subsequent transient stomatal closure and delayed recovery of photosystem II (PSII) quantum yield. Longer and hotter heat pulses resulted in sustained inhibition of photosynthesis, primarily due to reduced PSII activity. However, cellular damage as indicated by increased membrane conductivity was not found below 50 °C. These data demonstrate that aspen is remarkably resistant to short-term heat pulses that are frequent under strongly fluctuating light regimes. Although the heat pulses did not result in cellular damage, heatflecks can significantly reduce the whole plant carbon gain in the field due to the delayed photosynthetic recovery after the heat pulse.

[1]  Lingling Zhu,et al.  Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes. , 2018, Plant, cell & environment.

[2]  Ü. Niinemets When leaves go over the thermal edge. , 2018, Plant, cell & environment.

[3]  I. C. Prentice,et al.  Global climatic drivers of leaf size , 2017, Science.

[4]  P. Reich,et al.  Thermal limits of leaf metabolism across biomes , 2017, Global change biology.

[5]  Ü. Niinemets,et al.  Mono- and sesquiterpene release from tomato (Solanum lycopersicum) leaves upon mild and severe heat stress and through recovery: from gene expression to emission responses. , 2016, Environmental and experimental botany.

[6]  Ü. Niinemets,et al.  Spectacular Oscillations in Plant Isoprene Emission under Transient Conditions Explain the Enigmatic CO2 Response1 , 2016, Plant Physiology.

[7]  Ü. Niinemets,et al.  How specialized volatiles respond to chronic and short-term physiological and shock heat stress in Brassica nigra. , 2016, Plant, cell & environment.

[8]  Jizhong Zhou,et al.  Plant Thermoregulation: Energetics, Trait-Environment Interactions, and Carbon Economics. , 2015, Trends in ecology & evolution.

[9]  L. Tran,et al.  Regulation of Photosynthesis during Abiotic Stress-Induced Photoinhibition. , 2015, Molecular plant.

[10]  Ü. Niinemets,et al.  Photosynthetic responses to stress in Mediterranean evergreens: Mechanisms and models , 2014 .

[11]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[12]  S. Palmroth,et al.  Modelling photosynthesis in highly dynamic environments: the case of sunflecks. , 2012, Tree physiology.

[13]  R. W. Pearcy,et al.  Sunflecks in trees and forests: from photosynthetic physiology to global change biology. , 2012, Tree physiology.

[14]  L. Copolovici,et al.  Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. , 2012, Journal of plant physiology.

[15]  M. Tobias,et al.  Temperature responses of dark respiration in relation to leaf sugar concentration. , 2012, Physiologia plantarum.

[16]  U. Niinemets,et al.  When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H₂O₂ formation. , 2011, Plant, cell & environment.

[17]  N. McDowell,et al.  A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests , 2010 .

[18]  L. Pärn,et al.  Above-ground biomass characteristics of young hybrid aspen (Populus tremula L. x P. tremuloides Michx.) plantations on former agricultural land in Estonia , 2009 .

[19]  T. Sharkey,et al.  Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves. , 2009, Plant, cell & environment.

[20]  Thomas D. Sharkey,et al.  Photosynthetic electron transport and proton flux under moderate heat stress , 2009, Photosynthesis Research.

[21]  J. Kruk,et al.  Function of plastoquinone in heat stress reactions of plants. , 2008, Biochimica et biophysica acta.

[22]  R. Sage,et al.  The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. , 2008, Plant, cell & environment.

[23]  Norio Murata,et al.  How do environmental stresses accelerate photoinhibition? , 2008, Trends in plant science.

[24]  P. Eliáš Stomatal oscillations in adult forest trees in natural environment , 2008, Biologia Plantarum.

[25]  A. Tullus,et al.  Early growth of hybrid aspen (Populus × wettsteinii Hämet-Ahti) plantations on former agricultural lands in Estonia , 2007 .

[26]  Stephen M. Schrader,et al.  Rapid heating of intact leaves reveals initial effects of stromal oxidation on photosynthesis. , 2007, Plant, cell & environment.

[27]  Fernando Valladares,et al.  4 The Architecture of PlantCrowns : From Design Rules to Light Capture and Performance , 2007 .

[28]  R. Lemeur,et al.  Stomatal oscillations in orange trees under natural climatic conditions. , 2006, Annals of botany.

[29]  Thomas D. Sharkey,et al.  Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene , 2005 .

[30]  A. Portis,et al.  Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. , 2005, Plant & cell physiology.

[31]  R. Strasser,et al.  Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.). , 2005, Journal of plant physiology.

[32]  P. Haldimann,et al.  Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat‐dependent reduction of the activation state of ribulose‐1,5‐bisphosphate carboxylase/oxygenase , 2004 .

[33]  Stephen M. Schrader,et al.  Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature , 2004 .

[34]  Stephen M. Schrader,et al.  Thylakoid membrane responses to moderately high leaf temperature in Pima cotton , 2004 .

[35]  Tania June,et al.  A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. , 2004, Functional plant biology : FPB.

[36]  Michael E. Salvucci,et al.  Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. , 2004, Physiologia plantarum.

[37]  Y. Kashino,et al.  Effects of high temperatures on the photosynthetic systems in spinach: Oxygen-evolving activities, fluorescence characteristics and the denaturation process , 1998, Photosynthesis Research.

[38]  R. Strasser,et al.  Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light , 1991, Planta.

[39]  O. Lange,et al.  Determination of leaf heat resistance: comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods , 1984, Oecologia.

[40]  D. Young,et al.  Influence of sunflecks on the temperature and water relations of two subalpine understory congeners , 1979, Oecologia.

[41]  T. Sharkey,et al.  Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase , 2004, Photosynthesis Research.

[42]  S. Lutts,et al.  The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat , 2004, Plant Growth Regulation.

[43]  A. Leakey,et al.  High-temperature inhibition of photosynthesis is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling , 2003 .

[44]  Ü. Niinemets,et al.  Do the capacity and kinetics for modification of xanthophyll cycle pool size depend on growth irradiance in temperate trees , 2003 .

[45]  Paula Scotti Campos,et al.  Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. , 2003, Journal of plant physiology.

[46]  A. Laisk,et al.  A computer‐operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves , 2002 .

[47]  M. Nachit,et al.  The tolerance of PSII to high temperatures in durum wheat (T. turgidum conv. durum): genetic variation and relationship with yield under heat stress. , 2000 .

[48]  Kristine D. Johnson,et al.  Kinetics of leaf temperature fluctuation affect isoprene emission from red oak (Quercus rubra) leaves. , 1999, Tree physiology.

[49]  Ü. Niinemets,et al.  Shape of leaf photosynthetic electron transport versus temperature response curve is not constant along canopy light gradients in temperate deciduous trees , 1999 .

[50]  T. Sharkey,et al.  The regulation of isoprene emission responses to rapid leaf temperature fluctuations , 1998 .

[51]  G. Harris,et al.  Interaction between photon flux density and elevated temperatures on photoinhibition in Alocasia macrorrhiza , 1998, Planta.

[52]  F. Loreto,et al.  THERMOINHIBITION OF PHOTOSYNTHESIS AS ANALYZED BY GAS EXCHANGE AND CHLOROPHYLL FLUORESCENCE , 1998 .

[53]  K. Winter,et al.  High Photosynthetic Capacity in a Shade-Tolerant Crassulacean Acid Metabolism Plant (Implications for Sunfleck Use, Nonphotochemical Energy Dissipation, and Susceptibility to Photoinhibition) , 1997, Plant physiology.

[54]  I. E. Woodrow,et al.  Responses of Rainforest Understorey Plants to Excess Light during Sunflecks , 1997 .

[55]  A. Knapp,et al.  Leaf-level responses to light and temperature in two co-occurring Quercus (Fagaceae) species: implications for tree distribution patterns , 1994 .

[56]  Robert W. Pearcy,et al.  The effect of flutter on the temperature of poplar leaves and its implications for carbon gain , 1993 .

[57]  M. Havaux Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures , 1993 .

[58]  U. Heber,et al.  Oscillations in photosynthesis and reduction of photosystem 1 acceptor side in sunflower leaves. Functional cytochrome b6/f-photosystem 1 ferredoxin-NADP reductase supercomplexes , 1992 .

[59]  R. W. Pearcy,et al.  Interactions between Acclimation and Photoinhibition of Photosynthesis of a Tropical Forest Understorey Herb, Alocasia macrorrhiza, during Simulated Canopy Gap Formation , 1992 .

[60]  T. Whitlow,et al.  An improved method for using electrolyte leakage to assess membrane competence in plant tissues. , 1992, Plant physiology.

[61]  Robert W. Pearcy,et al.  SUNFLECKS AND PHOTOSYNTHESIS IN PLANT CANOPIES , 1990 .

[62]  P. Low,et al.  Identification and Partial Characterization of the Denaturation Transition of the Photosystem II Reaction Center of Spinach Chloroplast Membranes. , 1989, Plant physiology.

[63]  John Grace,et al.  3. Plant response to wind , 1988 .

[64]  W. Bilger,et al.  Chlorophyll fluorescence as an indicator of heat induced limitation of photosynthesis in Arbutus unedo L. , 1987 .

[65]  H. R. Holbo,et al.  Solar radiation at seedling sites below partial canopies , 1985 .

[66]  J. Berry,et al.  Photosynthetic response and adaptation to high temperature in desert plants : a comparison of gas exchange and fluorescence methods for studies of thermal tolerance. , 1984, Plant physiology.

[67]  J. Berry,et al.  Photosynthetic Response and Adaptation to Temperature in Higher Plants , 1980 .

[68]  John L. Monteith,et al.  Plant Response to Wind. , 1979 .